Mechanism of the electron transfer catalyst DsbB from Escherichia coli

EMBO Journal

Volumn 22, Issue 14, 2003, Pages 3503-3513

  Grauschopf, Ulla ^a   Fritz, Andrea ^a   Glockshuber, Rudi ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Disulfide bond formation; DsbA; DsbB; Redox potential; Ubiquinone

Indexed keywords

MEMBRANE PROTEIN; PROTEIN DSBB; UBIQUINONE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CATALYST; CHEMICAL REACTION KINETICS; DISULFIDE BOND; ELECTRON TRANSPORT; ESCHERICHIA COLI; MOLECULAR INTERACTION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REACTION ANALYSIS; REDUCTION;

BACTERIAL PROTEINS; CATALYSIS; CYSTEINE; DISULFIDES; ELECTRON TRANSPORT; ESCHERICHIA COLI; KINETICS; MEMBRANE PROTEINS; PROTEIN DISULFIDE-ISOMERASE; THERMODYNAMICS; VARIATION (GENETICS);

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0042815104     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg356     Document Type: Article

References (40)

1. Bader, M., Muse, W., Zander, T. and Bardwell, J. (1998) Reconstitution of a protein disulfide catalytic system. J. Biol. Chem., 273, 10302-10307.
2. Bader, M., Muse, W., Ballou, D.P., Gassner, C. and Bardwell, J.C. (1999) Oxidative protein folding is driven by the electron transport system. Cell, 98, 217-227.
3. Bader, M.W., Xie, T., Yu, C.A. and Bardwell, J.C. (2000) Disulfide bonds are generated by quinone reduction. J. Biol. Chem., 275, 26082-26088.
4. Bardwell, J.C., McGovern, K. and Beckwith, J. (1991) Identification of a protein required for disulfide bond formation in vivo. Cell, 67, 581-589.
5. Bardwell, J.C., Lee, J.O., Jander, G., Martin, N., Belin, D. and Beckwith, J. (1993) A pathway for disulfide bond formation in vivo. Proc. Natl Acad. Sci. USA, 90, 1038-1042.
6. Collet, J.F. and Bardwell, J.C. (2002) Oxidative protein folding in bacteria. Mol. Microbiol., 44, 1-8.
7. Dailey, F.E. and Berg, H.C. (1993) Mutants in disulfide bond formation that disrupt flagellar assembly in Escherichia coli. Proc. Natl Acad. Sci. USA, 90, 1043-1047.
8. Darby, N.J. and Creighton, T.E. (1995) Catalytic mechanism of DsbA and its comparison with that of protein disulfide isomerase. Biochemistry, 34, 3576-3587.
9. Debarbieux, L. and Beckwith, J. (2000) On the functional interchangeability, oxidant versus reductant, of members of the thioredoxin superfamily. J. Bacteriol., 182, 723-727.
10. Gennis, R.B. and Stewart, V. (1996) Escherichia coli and Salmonella - Cellular and Molecular Biology. ASM Press, Washington. DC.
11. Gill, S.C. and von Hippel, P.H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem., 182, 319-326.
12. Guddat, L.W., Bardwell, J.C. and Martin, J.L. (1998) Crystal structures of reduced and oxidized DsbA: investigation of domain motion and thiolate stabilization. Structure, 6, 757-767.
13. Guilhot, C., Jander, G., Martin, N.L. and Beckwith, J. (1995) Evidence that the pathway of disulfide bond formation in Escherichia coli involves interactions between the cysteines of DsbB and DsbA. Proc. Natl Acad. Sci. USA, 92, 9895-9899.
14. Hennecke, J., Sebbel, P. and Glockshuber, R. (1999) Random circular permutation of DsbA reveals segments that are essential for protein folding and stability. J. Mol. Biol., 286, 1197-1215.
15. Huber-Wunderlich, M. and Glockshuber, R. (1998) A single dipeptide sequence modulates the redox properties of a whole enzyme family. Fold. Des., 3, 161-171.
16. Inaba, K. and Ito, K. (2002) Paradoxical redox properties of DsbB and DsbA in the protein disulfide-introducing reaction cascade. EMBO J., 21, 2646-2654.
17. Jander, G., Martin, N.L. and Beckwith, J. (1994) Two cysteines in each periplasmic domain of the membrane protein DsbB are required for its function in protein disulfide bond formation. EMBO J., 13, 5121-5127.
18. Jonda, S., Huber-Wunderlich, M., Glockshuber, R. and Mössner E. (1999) Complementation of DsbA deficiency with secreted thioredoxin variants reveals the crucial role of an efficient dithiol oxidant for catalyzed protein folding in the bacterial periplasm. EMBO J., 18, 3271-3281.
19. Kadokura, H. and Beckwith, J. (2002) Four cysteines of the membrane protein DsbB act in concert to oxidize its substrate DsbA. EMBO J., 21, 2354-2363.
20. Kadokura, H., Bader, M., Tian, H., Bardwell, J.C. and Beckwith, J. (2000) Roles of a conserved arginine residue of DsbB in linking protein disulfide-bond-formation pathway to the respiratory chain of Escherichia coli. Proc. Natl Acad. Sci. USA, 97, 10884-10889.
21. Kadokura, H., Katzen, F. and Beckwith, J. (2003) Protein disulfide bond formation in procaryotes. Annu. Rev. Biochem., 72, 111-135.
22. Kishigami, S. and Ito, K. (1996) Roles of cysteine residues of DsbB in its activity to reoxidize DsbA, the protein disulphide bond catalyst of Escherichia coli. Genes Cells, 1, 201-208.
23. Kishigami, S., Kanaya, E., Kikuchi, M. and Ito, K. (1995) DsbA-DsbB interaction through their active site cysteines. Evidence from an odd cysteine mutant of DsbA. J. Biol. Chem., 270, 17072-17074.
24. Kobayashi, T. and Ito, K. (1999) Respiratory chain strongly oxidizes the CXXC motif of DsbB in the Escherichia coli disulfide bond formation pathway. EMBO J., 18, 1192-1198.
25. Kobayashi, T., Kishigami, S., Sone, M., Inokuchi, H., Mogi, T. and Ito, K. (1997) Respiratory chain is required to maintain oxidized states of the DsbA-DsbB disulfide bond formation system in aerobically growing Escherichia coli cells. Proc. Natl Acad. Sci. USA, 94, 11857-11862.
26. Kobayashi, T., Takahashi, Y. and Ito, K. (2001) Identification of a segment of DsbB essential for its respiration-coupled oxidation. Mol. Microbiol., 39, 158-165.
27. Kyte, J. (1995) Mechanism in Protein Chemistry. Garland Publishing, Inc., New York, NY, p. 373.
28. Meerman, H.J. and Georgiou, G. (1994) Construction and characterization of a set of E. coli strains deficient in all known loci affecting the proteolytic stability of secreted recombinant proteins. Biotechnology, 12, 1107-1110.
29. Missiakas, D., Georgopoulos, C. and Raina, S. (1993) Identification and characterization of the Escherichia coli gene dsbB, whose product is involved in the formation of disulfide bonds in vivo. Proc. Natl Acad. Sci. USA, 90, 7084-7088.
30. Mössner, E., Iwai, H. and Glockshuber, R. (2000) Influence of the pK(a) value of the buried, active-site cysteine on the redox properties of thioredoxin-like oxidoreductases. FEBS Lett., 477, 21-26.
31. Nelson, J.W. and Creighton, T.E. (1994) Reactivity and ionization of the active site cysteine residues of DsbA, a protein required for disulfide bond formation in vivo. Biochemistry, 33, 5974-5983.
32. Ostermeier, M., De Sutter, K. and Georgiou, G. (1996) Eukaryotic protein disulfide isomerase complements Escherichia coli dsbA mutants and increases the yield of a heterologous secreted protein with disulfide bonds. J. Biol. Chem., 271, 10616-10622.
33. Regeimbal, J. and Bardwell, J.C. (2002) DsbB catalyzes disulfide bond formation de novo. J. Biol. Chem., 277, 32706-32713.
34. Riddles, P.W., Blakeley, R.L. and Zerner, B. (1983) Reassessment of Ellman's reagent. Methods Enzymol., 91, 49-60.
35. Sevier, C.S. and Kaiser, C.A. (2002) Formation and transfer of disulphide bonds in living cells. Nat. Rev. Mol. Cell Biol., 3, 836-847.
36. Szajewski, R.P. and Whitesides, G.M. (1980) Rate constants and equilibrium constants for thiol-disulfide interchange reactions involving oxidized glutathione. J. Am. Chem. Soc., 102, 2011-2026.
37. Wunderlich, M. and Glockshuber, R. (1993) Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli. Protein Sci., 2, 717-726.
38. Wunderlich, M., Otto, A., Seckler, R. and Glockshuber, R. (1993) Bacterial protein disulfide isomerase: efficient catalysis of oxidative protein folding at acidic pH. Biochemistry, 32, 12251-12256.
39. Zapun, A. and Creighton, T.E. (1994) Effects of DsbA on the disulfide folding of bovine pancreatic trypsin inhibitor and alpha-lactalbumin. Biochemistry, 33, 5202-5211.
40. Zapun, A., Bardwell, J.C. and Creighton, T.E. (1993) The reactive and destabilizing disulfide bond of DsbA, a protein required for protein disulfide bond formation in vivo. Biochemistry, 32, 5083-5092.